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Microbial Community Response of an Organohalide Respiring Enrichment Culture to Permanganate Oxidation.

Sutton NB, Atashgahi S, Saccenti E, Grotenhuis T, Smidt H, Rijnaarts HH - PLoS ONE (2015)

Bottom Line: In contrast, high permanganate treatment disrupted dechlorination beyond cis-dichloroethene and caused at least a 2-4 orders of magnitude reduction in the abundance of all measured OHRB and rdh genes, as compared to the biotic control.High permanganate treatments resulted in a notably divergent microbial community, with increased abundances of organisms affiliated with Campylobacterales and Oceanospirillales capable of dissimilatory Mn reduction, and decreased abundance of presumed supporters of OHRB.Overall, this detailed investigation into dose-dependent changes of microbial composition and activity due to permanganate treatment provides insight into the mechanisms of OHR stimulation or disruption upon chemical oxidation.

View Article: PubMed Central - PubMed

Affiliation: Environmental Technology, Wageningen University, Wageningen, The Netherlands.

ABSTRACT
While in situ chemical oxidation is often used to remediate tetrachloroethene (PCE) contaminated locations, very little is known about its influence on microbial composition and organohalide respiration (OHR) activity. Here, we investigate the impact of oxidation with permanganate on OHR rates, the abundance of organohalide respiring bacteria (OHRB) and reductive dehalogenase (rdh) genes using quantitative PCR, and microbial community composition through sequencing of 16S rRNA genes. A PCE degrading enrichment was repeatedly treated with low (25 μmol), medium (50 μmol), or high (100 μmol) permanganate doses, or no oxidant treatment (biotic control). Low and medium treatments led to higher OHR rates and enrichment of several OHRB and rdh genes, as compared to the biotic control. Improved degradation rates can be attributed to enrichment of (1) OHRB able to also utilize Mn oxides as a terminal electron acceptor and (2) non-dechlorinating community members of the Clostridiales and Deltaproteobacteria possibly supporting OHRB by providing essential co-factors. In contrast, high permanganate treatment disrupted dechlorination beyond cis-dichloroethene and caused at least a 2-4 orders of magnitude reduction in the abundance of all measured OHRB and rdh genes, as compared to the biotic control. High permanganate treatments resulted in a notably divergent microbial community, with increased abundances of organisms affiliated with Campylobacterales and Oceanospirillales capable of dissimilatory Mn reduction, and decreased abundance of presumed supporters of OHRB. Although OTUs classified within the OHR-supportive order Clostridiales and OHRB increased in abundance over the course of 213 days following the final 100 μmol permanganate treatment, only limited regeneration of PCE dechlorination was observed in one of three microcosms, suggesting strong chemical oxidation treatments can irreversibly disrupt OHR. Overall, this detailed investigation into dose-dependent changes of microbial composition and activity due to permanganate treatment provides insight into the mechanisms of OHR stimulation or disruption upon chemical oxidation.

No MeSH data available.


Relative target abundance of OHRB (based on 16S rRNA gene) and rdh genes measured by qPCR.Values indicate the enrichment or reduction of a target relative to that measured in the biotic control. Data is averaged between duplicate microcosms for each time point prior to comparison with the biotic control. Error bars are the propagation of standard deviation in triplicate assays, averaging of duplicates, and calculation of relative abundance. (A) Results in low or medium permanganate treated microcosms are compared to results from the biotic control at the same time point. (B) Results from the high permanganate microcosms were compared to the biotic control on day 13 (H1+H2) and day 21 (H3+H4, H5+H6). H7, H8, and H9 are not included, as biotic controls are not available for these time points. Note that different concentration scales are used for Y axes of (A) and (B) panels.
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pone.0134615.g003: Relative target abundance of OHRB (based on 16S rRNA gene) and rdh genes measured by qPCR.Values indicate the enrichment or reduction of a target relative to that measured in the biotic control. Data is averaged between duplicate microcosms for each time point prior to comparison with the biotic control. Error bars are the propagation of standard deviation in triplicate assays, averaging of duplicates, and calculation of relative abundance. (A) Results in low or medium permanganate treated microcosms are compared to results from the biotic control at the same time point. (B) Results from the high permanganate microcosms were compared to the biotic control on day 13 (H1+H2) and day 21 (H3+H4, H5+H6). H7, H8, and H9 are not included, as biotic controls are not available for these time points. Note that different concentration scales are used for Y axes of (A) and (B) panels.

Mentions: To account for natural shifts in target gene abundance during the course of the experiment, the abundance of each target gene observed in microcosms receiving permanganate was normalized to the corresponding target gene in the biotic controls at each time point (Fig 3). Overall higher total bacteria and Geobacter normalized abundances were observed in microcosms receiving low and medium permanganate treatments. In the case of Geobacter, a well-described Mn reducer [38], 3–6 times higher abundances were measured on days 7, 13, and 21 in microcosms receiving medium permanganate treatment than in the biotic control (Fig 3A). During the first two weeks, a slight enrichment of D. mccartyi and vcrA was detected in microcosms receiving low or medium permanganate treatments. However, at the last sampling time point on day 21, the abundances of both targets were lower than those of the biotic control. Desulfitobacterium, bvcA, and tceA were consistently lower in permanganate treated microcosms than in the biotic controls (Fig 3A). In the case of bvcA and tceA, this result was particularly noteworthy considering the higher PCE degradation rate observed in permanganate treated microcosms (S1 Fig).


Microbial Community Response of an Organohalide Respiring Enrichment Culture to Permanganate Oxidation.

Sutton NB, Atashgahi S, Saccenti E, Grotenhuis T, Smidt H, Rijnaarts HH - PLoS ONE (2015)

Relative target abundance of OHRB (based on 16S rRNA gene) and rdh genes measured by qPCR.Values indicate the enrichment or reduction of a target relative to that measured in the biotic control. Data is averaged between duplicate microcosms for each time point prior to comparison with the biotic control. Error bars are the propagation of standard deviation in triplicate assays, averaging of duplicates, and calculation of relative abundance. (A) Results in low or medium permanganate treated microcosms are compared to results from the biotic control at the same time point. (B) Results from the high permanganate microcosms were compared to the biotic control on day 13 (H1+H2) and day 21 (H3+H4, H5+H6). H7, H8, and H9 are not included, as biotic controls are not available for these time points. Note that different concentration scales are used for Y axes of (A) and (B) panels.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4526698&req=5

pone.0134615.g003: Relative target abundance of OHRB (based on 16S rRNA gene) and rdh genes measured by qPCR.Values indicate the enrichment or reduction of a target relative to that measured in the biotic control. Data is averaged between duplicate microcosms for each time point prior to comparison with the biotic control. Error bars are the propagation of standard deviation in triplicate assays, averaging of duplicates, and calculation of relative abundance. (A) Results in low or medium permanganate treated microcosms are compared to results from the biotic control at the same time point. (B) Results from the high permanganate microcosms were compared to the biotic control on day 13 (H1+H2) and day 21 (H3+H4, H5+H6). H7, H8, and H9 are not included, as biotic controls are not available for these time points. Note that different concentration scales are used for Y axes of (A) and (B) panels.
Mentions: To account for natural shifts in target gene abundance during the course of the experiment, the abundance of each target gene observed in microcosms receiving permanganate was normalized to the corresponding target gene in the biotic controls at each time point (Fig 3). Overall higher total bacteria and Geobacter normalized abundances were observed in microcosms receiving low and medium permanganate treatments. In the case of Geobacter, a well-described Mn reducer [38], 3–6 times higher abundances were measured on days 7, 13, and 21 in microcosms receiving medium permanganate treatment than in the biotic control (Fig 3A). During the first two weeks, a slight enrichment of D. mccartyi and vcrA was detected in microcosms receiving low or medium permanganate treatments. However, at the last sampling time point on day 21, the abundances of both targets were lower than those of the biotic control. Desulfitobacterium, bvcA, and tceA were consistently lower in permanganate treated microcosms than in the biotic controls (Fig 3A). In the case of bvcA and tceA, this result was particularly noteworthy considering the higher PCE degradation rate observed in permanganate treated microcosms (S1 Fig).

Bottom Line: In contrast, high permanganate treatment disrupted dechlorination beyond cis-dichloroethene and caused at least a 2-4 orders of magnitude reduction in the abundance of all measured OHRB and rdh genes, as compared to the biotic control.High permanganate treatments resulted in a notably divergent microbial community, with increased abundances of organisms affiliated with Campylobacterales and Oceanospirillales capable of dissimilatory Mn reduction, and decreased abundance of presumed supporters of OHRB.Overall, this detailed investigation into dose-dependent changes of microbial composition and activity due to permanganate treatment provides insight into the mechanisms of OHR stimulation or disruption upon chemical oxidation.

View Article: PubMed Central - PubMed

Affiliation: Environmental Technology, Wageningen University, Wageningen, The Netherlands.

ABSTRACT
While in situ chemical oxidation is often used to remediate tetrachloroethene (PCE) contaminated locations, very little is known about its influence on microbial composition and organohalide respiration (OHR) activity. Here, we investigate the impact of oxidation with permanganate on OHR rates, the abundance of organohalide respiring bacteria (OHRB) and reductive dehalogenase (rdh) genes using quantitative PCR, and microbial community composition through sequencing of 16S rRNA genes. A PCE degrading enrichment was repeatedly treated with low (25 μmol), medium (50 μmol), or high (100 μmol) permanganate doses, or no oxidant treatment (biotic control). Low and medium treatments led to higher OHR rates and enrichment of several OHRB and rdh genes, as compared to the biotic control. Improved degradation rates can be attributed to enrichment of (1) OHRB able to also utilize Mn oxides as a terminal electron acceptor and (2) non-dechlorinating community members of the Clostridiales and Deltaproteobacteria possibly supporting OHRB by providing essential co-factors. In contrast, high permanganate treatment disrupted dechlorination beyond cis-dichloroethene and caused at least a 2-4 orders of magnitude reduction in the abundance of all measured OHRB and rdh genes, as compared to the biotic control. High permanganate treatments resulted in a notably divergent microbial community, with increased abundances of organisms affiliated with Campylobacterales and Oceanospirillales capable of dissimilatory Mn reduction, and decreased abundance of presumed supporters of OHRB. Although OTUs classified within the OHR-supportive order Clostridiales and OHRB increased in abundance over the course of 213 days following the final 100 μmol permanganate treatment, only limited regeneration of PCE dechlorination was observed in one of three microcosms, suggesting strong chemical oxidation treatments can irreversibly disrupt OHR. Overall, this detailed investigation into dose-dependent changes of microbial composition and activity due to permanganate treatment provides insight into the mechanisms of OHR stimulation or disruption upon chemical oxidation.

No MeSH data available.